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European Journal of Applied Physiology

, Volume 110, Issue 4, pp 845–851 | Cite as

Low-volume strength and endurance training prevent the decrease in exercise hyperemia induced by non-dominant forearm immobilization

  • Fumiko Ohmori
  • Takafumi HamaokaEmail author
  • Kiyoshi Shiroishi
  • Takuya Osada
  • Norio Murase
  • Yuko Kurosawa
  • Shiro Ichimura
  • Toshiyuki Homma
  • Kazuki Esaki
  • Ryotaro Kime
  • Toshihito Katsumura
Original Article

Abstract

We examined the effect of 3-week upper limb immobilization on conduit artery cross-sectional area and peak hyperemia (BFpeak) after exhaustive dynamic handgrip exercise (Exdyn), and that of low-volume strength and endurance training during immobilization. Healthy volunteers (n = 21; mean age, 22 years) were divided into 3 groups: immobilization only (IMM; n = 7), immobilization with training (STR + END; n = 7), and control (no immobilization or training, CNT; n = 7). Endurance training comprised Exdyn at 30% maximum voluntary contraction (MVC) (duration of each session, ~60 s; twice weekly). Strength training involved intermittent isometric handgrip exercise at 70% MVC (duration of each session, 40 s; twice weekly), repeated 10 times. We used ultrasound methods to measure the brachial artery cross-sectional area and the BFpeak after Exdyn for 5 min pre- and post-immobilization. We found a significant group by time interaction in BFpeak (p < 0.05). A significant decrease was found in BFpeak in the IMM (p < 0.05) between pre- and post-immobilization and a protective effect in the STR + END. The 3-week upper limb immobilization did not influence the baseline artery cross-sectional area. In conclusion, BFpeak decreased after 3-week upper limb immobilization and a combination of strength training and endurance training preserved the blunted BFpeak.

Keywords

Hyperemic response Immobilization Strength and endurance training Grip exercise 

Introduction

Muscle disuse induces its structural and functional adaptation, such as reduced muscle mass and strength (Convertino et al. 1989; Edgerton et al. 1995) and a decrease in endurance (Kitahara et al. 2003; Mulder et al. 2007), as well as vascular remodeling (Beere et al. 1999; Bleeker et al. 2005b). Vascular dysfunction associated with physical inactivity is a risk factor for cardiovascular diseases (Thijssen et al. 2010). Therefore, it is important to find an intervention method for preserving structural and functional deterioration due to the muscle disuse. Finding the effective intervention would also be helpful in developing exercise programs for rehabilitation during the early post-surgery period in order to minimize the deleterious effects of disuse atrophy. An intervention method would also be applicable in the treatment of astronauts in space flight since it would counter hemodynamic dysfunction and preserve strength.

Previous studies have evaluated the effect of muscle disuse on resting arterial diameter and blood flow (Bleeker et al. 2005b; Kamiya et al. 2000), reactive hyperemic blood flow (Bleeker et al. 2005a), and blood flow response to muscle contractions (McDonald et al. 1992; Mulder et al. 2007; Woodman et al. 1995). Although animal studies have been conducted on the effects of short-term disuse on the blood flow response to a metabolic challenge (McDonald et al. 1992; Tyml et al. 1995, 1999), limited information is available on the effects of disuse (Mulder et al. 2007) in humans.

Various models of disuse have been chosen, such as bed rest (Mulder et al. 2007), space flight (Edgerton et al. 1995), leg suspension (Berg et al. 1991, 1993; Bleeker et al. 2005a) spinal cord injury (De Groot et al. 2003), leg immobilization (McComas 1994), and upper limb immobilization (Kitahara et al. 2003; Motobe et al. 2004). In this study, we chose the 3-week upper limb immobilization that can specifically induce the functional decline of muscles (Matsumura et al. 2008; Motobe et al. 2004; Homma et al. 2009), but does not cause any muscle mass reduction (Kitahara et al. 2003). With respect to preserving muscle functions, it has been reported that a combination of low-volume strength and endurance training is effective in preserving muscle strength, endurance, and oxidative capacity (Matsumura et al. 2008). However, previous studies have not examined the effects of immobilization on the structural and functional changes of the conduit artery or the effects of exercise training on preventing blood flow deterioration.

Therefore, the purpose of this study was to examine the effect of disuse using 3-week upper limb immobilization on the structure of the conduit artery and peak exercise hyperemia. In addition, the study evaluated the potential protective effect of low-volume strength and/or endurance training during immobilization on the conduit artery and peak exercise hyperemia. We hypothesized that 3-week upper limb immobilization would not decrease baseline artery diameter and blood flow, and would decrease exhaustive exercise-induced hyperemic response. We also hypothesized that a combination of endurance and strength training would have a protective effect on the deteriorated function.

Materials and methods

The study subjects were 21 healthy men. The experiment was conducted after the protocol was reviewed by the ethical committee of the National Space Development Agency of Japan (NASDA), and after obtaining informed consent from the subjects. For subjects of the immobilization group and training group, the non-dominant arm was immobilized for 21 days in a cast. The cast was applied from the fingers to two-thirds of the upper arm in the natural position. Subjects were instructed to wear slings in the daytime, except when changing clothes and bathing. Furthermore, they were unable to remove the cast by themselves during the study. The subjects were randomly divided into the following 3 groups: immobilization only (IMM; 7 subjects, 22.9 ± 2.9 years, 172.8 ± 6.6 cm, and 70.0 ± 12.9 kg), immobilization with endurance and strength training (STR + END; 7 subjects, 22.1 ± 4.0 years, 172.5 ± 5.0 cm, and 65.8 ± 10.3 kg) performed twice weekly, and control or no immobilization or training group (CNT; 7 subjects, 21.1 ± 0.9 years, 172.2 ± 3.0 cm, and 66.0 ± 11.1 kg). We measured the following parameters for participants in all groups before and after the 21-day immobilization: forearm circumference, grip MVC, and grip endurance with blood flow monitoring.

Experimental protocols

Each subject sat in an upright position with his arm in the horizontal position; the forearm circumference of each subject followed by the grip maximum voluntary contraction (MVC) was measured. Following a 10-min rest period, baseline measurement was conducted of the cross-sectional area of the vessel and the blood velocity. Five minutes after the baseline measurement, the subjects started exercise testing (~60 s) and kept returning to the resting position for 5 min after every round of exercise.

Physiological measurements

Each subject sat in an upright position with his arm in the horizontal position and performed handgrip isotonic contractions at a 1 Hz until exhaustion (Exdyn) while using a handgrip ergometer. The subjects lifted a mass for a distance of 2 cm adjusted to 30% of the MVC measured before and after immobilization (lifted a mass during the first 0.5 s, and lowered it during the subsequent 0.5 s). The subjects were instructed to stop exercise by the researcher when the subjects could not keep up with a metronome set at 1-s intervals. Then, the end point of the exercise was determined retrospectively by the time recorded in a stopwatch. This end point was recorded as the grip endurance, expressed as the number of handgrip contractions; throughout the experiment, this endpoint was judged by the same researcher.

Forearm circumference was measured at the largest point of the forearm. The site of the initial measurement was marked, and care was taken to measure at the same site after immobilization. Isometric MVC was measured using an analogue grip dynamometer (Takei Kiki Kogyo, Japan) before the endurance test was performed. Three measurements were made, and the largest was considered as the MVC value.

The mean blood velocity (V mean) and vessel diameter of the brachial artery were measured using Doppler and B-mode ultrasound imaging (Logic 3, General Electric, USA). A 10-MHz linear array transducer was placed on the skin over a brachial artery just proximal to the elbow. The sampling volume was maintained at 4.5 mm, and the angle of the beam used to determine the direction of the blood flow was automatically adjusted to 60°.

The diameter of the blood vessel considering the relative time periods of the systolic (1/3) and diastolic (2/3) phases of the cardiac cycle was assumed to be the most representative diameter size in each cardiac cycle (Rådegran and Saltin 1998). This value was used to determine the cross-sectional area of the vessel (area = πr 2, where r is the radius of the vessel) and to calculate the blood flow. Beat-by-beat brachial artery blood flow was calculated by multiplying V mean and πr 2.

The shear stress was calculated using the equation 4ηV mean/diameter, where η is the blood viscosity (assumed as 4.0 cP). The resting blood flow was calculated as the average of 10 pulse beats during resting conditions before exercise. The hyperemic response during recovery was monitored for 5 min following Exdyn. Data were averaged using 5 pulse beats each immediately before the 5th, 10th, 20th, 30th, 60th, 90th, 120th, 150th, 180th, 240th, and 300th second during the recovery period after exercise. The peak hyperemia (BFpeak) was defined as the highest value (the average of 5-pulse beats) during recovery.

Training

The strength training consisted of intermittent isometric handgrip exercises at 70% MVC for 2 s with a 2-s rest interval, repeated 10 times. The setup for performing grip exercise was the same as mentioned in the exercise testing section. The endurance training regimen was the same as Exdyn mentioned in the exercise testing section. Strength and endurance training were performed twice weekly by the subjects of the STR + END group during immobilization. First, strength training was performed (duration of each session, ~40 s), and 30 min thereafter, endurance training was performed (duration of each session, ~60 s).

Statistical analysis

The measurement values of each group are expressed as mean ± SD. We evaluated the differences between the pre- and post-immobilization values of forearm circumference, MVC, grip endurance, and basal artery diameter, blood flow, and shear stress, and BFpeak of the 3 groups by using two-way (group by time) repeated measures analysis of variance (ANOVA) (SPSS vol. 15.0J). When a significant interaction or a main effect of factor 1 (time) or factor 2 (group), we performed post hoc comparison between pre- and post-immobilization by using Tukey’s HSD test. A p value of less than 0.05 was considered statistically significant.

Results

At the baseline, for all the measurements made before immobilization, no significant difference was observed between the groups. We did not find any significant group-by-pre-post immobilization interactions for forearm circumference (CNT: pre 25.3 ± 0.5 cm, post 25.3 ± 0.5 cm; IMM: pre 25.3 ± 0.6 cm, post 25.2 ± 0.6 cm; STR + END: pre 24.4 ± 0.5 cm, post 24.6 ± 0.6 cm). As shown in Fig. 1, a significant immobilization interaction (p < 0.05) was observed for MVC between the groups [CNT: pre 42.3 ± 3.1 kg, post 41.9 ± 2.6 kg (−0.2%); IMM: pre 41.1 ± 2.2 kg, post 33.2 ± 2.0 kg (−19.0%); STR + END: pre 39.5 ± 4.4 kg, post 40.6 ± 4.9 kg (2.2%)]. The post hoc comparison between pre- and post-immobilization MVC shows a significant decrease in the IMM (p < 0.05) and a protective effect in the STR + END. Grip endurance for all the groups is no significant interaction between the groups (CNT: pre 57.4 ± 3.1 s, post 59.9 ± 3.9 s; IMM: pre 63.4 ± 7.3 s, post 64.4 ± 2.1 s; STR + END: pre 58.3 ± 3.3 s, post 60.9 ± 5.6 s). Table 1 shows the pre- and post-immobilization values of vessel diameter, blood flow, and shear stress at rest for all the groups. No significant difference was observed in any baseline parameters before and after immobilization. A significant immobilization interaction (p < 0.05) was observed for BFpeak between the groups [(CNT: pre 391.1 ± 43.5 ml/min, post 400.1 ± 54.9 ml/min (0.8%); IMM: pre 487.0 ± 47.3 ml/min, post 367.6 ± 39.9 ml/min (−22.1%); STR + END: pre 457.4 ± 70.8 ml/min, post 560.0 ± 101.5 ml/min (21.8%)]. The post hoc comparison revealed a significant decrease in the IMM (p < 0.05) and a protective effect in the STR + END (Fig. 2).
Fig. 1

Maximum voluntary contraction (MVC) for all the groups before and after immobilization. Grip MVC was measured pre- and post-forearm immobilization (3 weeks). Asterisk a significant group-by-time immobilization interaction Hash the post hoc comparison between pre- and post-immobilization The groups were as follows: IMM immobilization, STR + END immobilization with endurance and strength training performed twice weekly, and CNT control (no immobilization or training)

Table 1

Vessel diameter, blood flow, and shear stress at rest for all the groups before and after a 3-week immobilization

 

Vessel diameter (cm)

Brachial blood flow (ml/min)

Shear stress (dynes/cm2)

Pre

Post

Pre

Post

Pre

Post

CNT

0.39 ± 0.01

0.39 ± 0.01

97.7 ± 10.0

82.5 ± 13.8

13.6 ± 1.3

11.5 ± 1.9

IMM

0.38 ± 0.01

0.36 ± 0.02

81.1 ± 19.1

73.7 ± 12.0

11.8 ± 2.8

12.9 ± 2.3

STR + END

0.40 ± 0.02

0.40 ± 0.01

76.9 ± 13.4

99.0 ± 27.7

10.9 ± 1.9

14.7 ± 4.6

No significant differences were found in any parameters between the groups before and after immobilization. The groups were as follows: IMM immobilization, STR + END immobilization with endurance and strength training performed twice weekly, CNT control (no immobilization or training)

Fig. 2

Peak blood flow for all the groups before and after immobilization. Peak blood flow was measured following exhaustive grip exercise at 30% maximal voluntary contraction pre- and post-forearm immobilization (3 weeks). Asterisk a significant group-by-time immobilization interaction. Hash the post hoc comparison between pre- and post-immobilization The groups were as follows: IMM immobilization, STR + END immobilization with endurance and strength training performed twice weekly, CNT control (no immobilization or training)

Discussion

The following hypotheses were primarily supported by our study: (1) exhaustive exercise-induced hyperemic response (BFpeak) decreases after 3-week upper limb immobilization and (2) a combination of endurance and strength training sustained this response. The baseline artery diameter, shear stress, and blood flow did not decrease after the 3-week upper limb immobilization.

Baseline vessel diameter and blood flow

We did not find any significant changes either in the diameter of the brachial artery or in the blood flow at rest during immobilization with and without training. Our observation is in contrast to the results of previous studies, which reported the decrease in the diameter of the brachial artery and in the blood flow (Kamiya et al. 2000; De Groot et al. 2004; Bleeker et al. 2005b). This dissociation is due, in part, to the model used (arm immobilization vs. leg immobilization or complete bed rest), i.e., the nature of immobilization in this experiment resulted in mild deconditioning and unaltered hydrostatic pressure. Blood flow to the arteries of the proximal limb could be adjusted according to the metabolic needs of the corresponding muscles (Huonker et al. 2003). Therefore, the vascular structure might have remained unchanged because the blood flow demand of the muscle remained unaltered, with unchanged muscle mass (Kitahara et al. 2003).

Blood flow response to exhaustive exercise

The reduction in contraction-induced hyperemia (Schrage et al. 2000; Woodman et al. 1995; McDonald et al. 1992) may be due to blunt vascular responsiveness to acetylcholine (Schrage et al. 2000) flow shear stress, nitric oxide (Jasperse et al. 1999; McCurdy et al. 2000), or adenosine (McCurdy et al. 2000) and due to the decrease in the number of capillaries or in capillary length (Ferretti et al. 1997). It is demonstrated that the effect of endothelin-1 (ET-1) contributes to the increased baseline vascular tone in the inactive legs of SCI individuals (Thijssen et al. 2007). It is speculated that, although there is no direct evidence on the effect of ET-1 on hyperemic response, this vasoconstrictor pathway might be involved in the blunt hyperemic response to a metabolic challenge observed in this study.

The amplitude of reduction (−39 to −35%) after 2 weeks of unloading (Woodman et al. 1995) is in accordance with our observations (24.5% reduction in peak blood flow). The changes in the amplitude and time course of post-exercise hyperemia before and after immobilization were similar to those reported for oxidative capacity (34% reduction) (Homma et al. 2009). It has been reported that constant load dynamic handgrip exercise training five sessions per week, each lasting nearly 1 min, is effective in improving muscle oxidative function in free-living healthy subjects (Hamaoka et al. 1998). In this study, we examined the effect of a lower-frequency training than that used in a previous study (Hamaoka et al. 1998) on preventing a decrease in muscle oxidative metabolism and endurance during muscle unloading.

Previous studies (McDonald et al. 1992; Overton et al. 1989) have hypothesized that the alteration in the blood flow distribution in the hindlimb musculature contributes to reduced aerobic capacity in animals. Although there was a significant correlation between the changes in oxidative capacity and endurance reported in the previous study (Homma et al. 2009), we did not find any significant correlation between these the changes in the endurance time and BFpeak in either group. It is possible that we did not find any correlations between endurance time and BFpeak because the absolute force for pre- and post-immobilization in the endurance test was different. Previous studies indicate a decrease in grip endurance at absolute intensity after a 3-week immobilization period, which might have led to an association between grip endurance and peak blood flow.

However, if we choose to use absolute force for an endurance test, the post-immobilization endurance time would decrease by 10–20%, according to previous studies (Kitahara et al. 2003; Homma et al. 2009). In this case, the decrease in endurance time itself should also influence a blunt hyperemic response. Therefore, we have decided to use relative force as a post-condition when the endurance time was almost equivalent between the pre- and post-conditions. Further research is needed to determine whether the reduced muscle blood flow contributes to the decrease in grip endurance or vice versa.

Functional tests

Strength

In previous studies, although there was no decrease in cross-sectional area of the forearm muscle after the 21-day forearm immobilization period (Kitahara et al. 2003), muscle strength was found to decrease from 15.6 to 18.2% (Kitahara et al. 2003; Matsumura et al. 2008; Motobe et al. 2004) (19.2% in this study) for grip contraction. A combination of strength and endurance training did have a preventative effect. The reduction in MVC associated with disuse could be attributed to deficits in both central activation (Clark et al. 2006) and contractile properties (Clark et al. 2008). Endurance training is generally not considered to produce a preventive effect on attenuated MVC, especially through the modification of contractile properties. Therefore, we speculate that the additive effect of endurance training on strength recovery may be due to an alteration of central properties or muscle recruitment. On the other hand, a dynamic leg extension training at 15.5% MVC for 12 weeks was reported to be effective in increasing muscle strength by 19% (Holm et al. 2008), indicating that a lower intensity training (30% MVC in this study) may possess the ability to enhance muscle strength.

Grip endurance

In this study, we did not find any significant decreases in grip endurance at relative (post-MVC) exercise intensity after the 3-week immobilization. Grip endurance has been shown to decrease from 18.3 to 19.5% in previous studies (Kitahara et al. 2003; Motobe et al. 2004) that tested grip endurance at absolute exercise intensity (pre-MVC) after a 3-week upper limb immobilization. There have been substantial studies on the effect of disuse on grip endurance or muscle fatigability reporting a reduction in performance (Berg et al. 1993; Veldhuizen et al. 1993) or no change (Fuglevand et al. 1995; Kamiya et al. 2004) or even increase in performance (Clark et al. 2008). The reason for the discrepancy between the present and some of the previous studies may be the difference in the muscle type tested (arm vs. leg, fast- vs. slow-twitch fibers), the methods used to generate muscle force (electrically evoked vs. voluntarily contracted), the contraction mode (isometric vs. dynamic), or the tension level in terms of absolute versus relative percentage of MVC before and after immobilization.

Limitations

Immobilization does not alter baseline mean systemic blood pressure in animals (McDonald et al. 1992; Tyml et al. 1999, 1995) and humans (Kamiya et al. 2004) as well as the exercise-induced blood pressure response in humans (Kamiya et al. 2004). Therefore, we speculated that the blood pressure response might not change after immobilization in this study. However, we did not measure the blood pressure response, which is a potential limitation of this study. We could not rule out the possibility that the augmented muscle sympathetic nerve activity (Kamiya et al. 2004) and the decreased endothelial functions (Bleeker et al. 2005b) after immobilization might be associated with the blunt hyperemic response.

Our previous study (Kitahara et al. 2003) determined that there were no differences in any muscle functions (i.e., CSA, MVC force, time course for PCr recovery, grip endurance, PCr or pH during a grip endurance test) between the dominant and non-dominant arms before the intervention and no changes in the muscle functions of the control arm after the intervention. The measurement methods and the intervention period of those studies were identical to those of the current study. Therefore, although true control was not present in the current study, we believe that the results of the current study are reliable and unaffected by day-to-day variations. However, it is possible that the intervention may influence subject’s habit and therefore influence both training response and daily physical activity level. If the dominant arm, which is more active than the non-dominant arm, was immobilized, the muscle cross-sectional area and functions might greatly decrease after immobilization.

Conclusion

In conclusion, the 3-week non-dominant upper limb immobilization did not change baseline artery structure, but decreased the hyperemic response to exhaustive exercise. During immobilization, a combination of low-volume strength training (40 s each, twice weekly) and endurance training (~60 s each, twice weekly) sustained the exhaustive exercise-induced hyperemic response.

Notes

Acknowledgments

The authors are grateful to all the volunteers who participated in this study. This work was supported, in part, by NASDA and a grant-in-aid from the Japanese Ministry of Education, Science, Sports and Culture.

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Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Fumiko Ohmori
    • 1
  • Takafumi Hamaoka
    • 1
    Email author
  • Kiyoshi Shiroishi
    • 2
  • Takuya Osada
    • 3
  • Norio Murase
    • 3
  • Yuko Kurosawa
    • 4
  • Shiro Ichimura
    • 5
  • Toshiyuki Homma
    • 6
  • Kazuki Esaki
    • 7
  • Ryotaro Kime
    • 3
  • Toshihito Katsumura
    • 3
  1. 1.National Institute of Fitness and Sports in KanoyaKanoyaJapan
  2. 2.Department of Judotherapy and Sports Medicine, Faculty of Health ScienceRyotokuji UniversityUrayasuJapan
  3. 3.Department of Sports Medicine for Health PromotionTokyo Medical UniversityTokyoJapan
  4. 4.Department of Neurology, Vontz Center for Molecular StudiesUniversity of CincinnatiCincinnatiUSA
  5. 5.Faculty of Science and TechnologyTokyo University of ScienceNodaJapan
  6. 6.Department of Sports ScienceJapan Institute of Sports SciencesTokyoJapan
  7. 7.Department of EducationShiga UniversityOhtsuJapan

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